Sodium channels contribute to degeneration of dorsal root ganglion neurites induced by mitochondrial dysfunction in an in vitro model of axonal injury

Journal of Neuroscience

Volumn 33, Issue 49, 2013, Pages 19250-19261

  Persson, Anna Karin ^a,b   Kim, Insil ^a,b   Zhao, Peng ^a,b   Estacion, Mark ^a,b   Black, Joel A ^a,b   Waxman, Stephen G ^a,b  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VA CONNECTICUT HEALTHCARE SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 [2 [4 (4 NITROBENZYLOXY) PHENYL] ETHYL] ISOTHIOUREA METHANESULFONATE; ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); ADENOSINE TRIPHOSPHATE; HYDROGEN PEROXIDE; OUABAIN; PEPTIDES AND PROTEINS; REACTIVE OXYGEN METABOLITE; ROTENONE; SODIUM CALCIUM EXCHANGE PROTEIN; TDTOMATO PROTEIN; TETRODOTOXIN; UNCLASSIFIED DRUG; VINCRISTINE; VOLTAGE GATED SODIUM CHANNEL;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AXONAL INJURY; CALCIUM HOMEOSTASIS; CELL DEATH; CELL STRESS; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENERGETIC STRESS; FEMALE; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MALE; MOUSE; NERVE DEGENERATION; NERVE FIBER DEGENERATION; NERVE FIBER GROWTH; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; SPINAL GANGLION;

ANIMALS; AXONS; AXOTOMY; CELL DEATH; CELLS, CULTURED; GANGLIA, SPINAL; HUMANS; HYDROGEN PEROXIDE; IMMUNOHISTOCHEMISTRY; MICE; MICE, TRANSGENIC; MICROTUBULES; MITOCHONDRIAL DISEASES; NERVE DEGENERATION; NEURITES; OXIDANTS; ROTENONE; SODIUM CHANNEL BLOCKERS; SODIUM CHANNELS; SODIUM-CALCIUM EXCHANGER; SODIUM-POTASSIUM-EXCHANGING ATPASE; TETRODOTOXIN; THIOUREA; UNCOUPLING AGENTS;

EID: 84889075974     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2148-13.2013     Document Type: Article

References (66)

1. 2+ exchanger. J Neurosci 16:545-552. Medline
2. Ames A 3rd (2000) CNS energy metabolism as related to function. Brain Res Brain Res Rev 34:42-68. CrossRef Medline
3. Arnold B, Cassady SJ, VanLaar VS, Berman SB (2011) Integrating multiple aspects of mitochondrial dynamics in neurons: age-related differences and dynamic changes in a chronic rotenone model. Neurobiol Dis 41: 189-200. CrossRef Medline
4. 2+-ATPase in pancreatic acinar cells: role of the mitochondria. Am J Physiol Cell Physiol 295:C1247-1260. CrossRef Medline
5. Bechtold DA, Yue X, Evans RM, Davies M, Gregson NA, Smith KJ (2005) Axonal protection in experimental autoimmune neuritis by the sodium channel blocking agent flecainide. Brain 128:18-28. CrossRef Medline
6. Bednarik J, Vlckova-Moravcova E, Bursova S, Belobradkova J, Dusek L, Sommer C (2009) Etiology of small-fiber neuropathy. J Peripher Nerv Syst 14:177-183. CrossRef Medline
7. 2+ efflux mechanisms following depolarization evoked calcium transients in cultured rat sensory neurones. J Physiol 455:567-583. Medline
8. Boyette-Davis JA, Cata JP, Driver LC, Novy DM, Bruel BM, Mooring DL, Wendelschafer-Crabb G, Kennedy WR, Dougherty PM (2013) Persistent chemoneuropathy in patients receiving the plant alkaloids paclitaxel and vincristine. Cancer Chemother Pharmacol 71:619-626. CrossRef Medline
9. Campbell GR, Ohno N, Turnbull DM, Mahad DJ (2012) Mitochondrial changes within axons in multiple sclerosis: an update. Curr Opin Neurol 25:221-230. CrossRef Medline
10. Campenot RB (1977) Local control of neurite development by nerve growth factor. Proc Natl Acad Sci U S A 74:4516-4519. CrossRef Medline
11. Campenot RB, Lund K, Mok SA (2009) Production of compartmented cultures of rat sympathetic neurons. Nat Protoc 4:1869-1887. CrossRef Medline
12. Carafoli E, Santella L, Branca D, Brini M (2001) Generation, control, and processing of cellular calcium signals. Crit Rev Biochem Mol Biol 36:107-260. CrossRef Medline
13. Catterall WA, Goldin AL, Waxman SG (2005) International Union of Pharmacology. XLVII. Nomenclature and structure-function relationships of voltage-gated sodium channels. Pharmacol Rev 57:397-409. CrossRef Medline
14. Chen H, Chan DC (2009) Mitochondrial dynamics-fusion, fission, movement, and mitophagy-in neurodegenerative diseases. Hum Mol Genet 18:R169-176. CrossRef Medline
15. Coleman MP, Freeman MR (2010) Wallerian degeneration, wld(s), and nmnat. Annu Rev Neurosci 33:245-267. CrossRef Medline
16. Courchesne SL, Karch C, Pazyra-Murphy MF, Segal RA (2011) Sensory neuropathy attributable to loss of Bcl-w. J Neurosci 31:1624-1634. CrossRef Medline
17. Court FA, Coleman MP (2012) Mitochondria as a central sensor for axonal degenerative stimuli. Trends Neurosci 35:364-372. CrossRef Medline
18. Cummins TR, Howe JR, Waxman SG (1998) Slow closed-state inactivation: a novel mechanism underlying ramp currents in cells expressing the hNE/ PN1 sodium channel. J Neurosci 18:9607-9619. Medline
19. Delettre C, Lenaers G, Griffoin JM, Gigarel N, Lorenzo C, Belenguer P, Pelloquin L, Grosgeorge J, Turc-Carel C, Perret E, Astarie-Dequeker C, Lasquellec L, Arnaud B, Ducommun B, Kaplan J, Hamel CP (2000) Nuclear gene OPA1, encoding a mitochondrial dynamin-related protein, is mutated in dominant optic atrophy. Nat Genet 26:207-210. CrossRef Medline
20. Dib-Hajj SD, Choi JS, Macala LJ, Tyrrell L, Black JA, Cummins TR, Waxman SG (2009) Transfection of rat or mouse neurons by biolistics or electroporation. Nat Protoc 4:1118-1126. CrossRef Medline
21. DiPolo R, Beaugé L (1979) Physiological role of ATP-driven calcium pump in squid axon. Nature 278:271-273. CrossRef Medline
22. Donnelly DF (2008) Spontaneous action potential generation due to persistent sodium channel currents in simulated carotid body afferent fibers. J Appl Physiol 104:1394-1401. CrossRef Medline
23. Dutta R, McDonough J, Yin X, Peterson J, Chang A, Torres T, Gudz T, Macklin WB, Lewis DA, Fox RJ, Rudick R, Mirnics K, Trapp BD (2006) Mitochondrial dysfunction as a cause of axonal degeneration in multiple sclerosis patients. Ann Neurol 59:478-489. CrossRef Medline
24. England JD, Asbury AK (2004) Peripheral neuropathy. Lancet 363:2151-2161. CrossRef Medline
25. Faber CG, Hoeijmakers JG, Ahn HS, Cheng X, Han C, Choi JS, Estacion M, Lauria G, Vanhoutte EK, Gerrits MM, Dib-Hajj S, Drenth JP, Waxman SG, Merkies IS (2012a) Gain of function Nanu1.7 mutations in idiopathic small fiber neuropathy. Ann Neurol 71:26-39. CrossRef Medline
26. Faber CG, Lauria G, Merkies IS, Cheng X, Han C, Ahn HS, Persson AK, Hoeijmakers JG, Gerrits MM, Pierro T, Lombardi R, Kapetis D, Dib-Hajj SD, Waxman SG (2012b) Gain-of-function Nav1.8 mutations in painful neuropathy. Proc Natl Acad Sci U S A 109:19444-19449. CrossRef Medline
27. Federico A, Cardaioli E, Da Pozzo P, Formichi P, Gallus GN, Radi E (2012) Mitochondria, oxidative stress and neurodegeneration. J Neurol Sci 322: 254-262. CrossRef Medline
28. Fern R, Ransom BR, Stys PK, Waxman SG (1993) Pharmacological protection of CNS white matter during anoxia: actions of phenytoin, carbamazepine and diazepam. J Pharmacol Exp Ther 266:1549-1555. Medline
29. Gover TD, Moreira TH, Kao JP, Weinreich D (2007) Calcium regulation in individual peripheral sensory nerve terminals of the rat. J Physiol 578: 481-490. CrossRef Medline
30. Hains BC, Waxman SG (2005) Neuroprotection by sodium channel blockade with phenytoin in an experimental model of glaucoma. Invest Ophthalmol Vis Sci 46:4164-4169. CrossRef Medline
31. Hains BC, Saab CY, Lo AC, Waxman SG (2004) Sodium channel blockade with phenytoin protects spinal cord axons, enhances axonal conduction, and improves functional motor recovery after contusion SCI. Exp Neurol 188:365-377. CrossRef Medline
32. Heitz FD, Erb M, Anklin C, Robay D, Pernet V, Gueven N (2012) Idebenone protects against retinal damage and loss of vision in a mouse model of Leber's hereditary optic neuropathy. PLoS One 7:e45182. CrossRef Medline
33. Huang Q, Wang H, Perry SW, Figueiredo-Pereira ME (2013) Negative regulation of 26S proteasome stability via calpain-mediated cleavage of Rpn10 subunit upon mitochondrial dysfunction in neurons. J Biol Chem 288:12161-12174. CrossRef Medline
34. Kaptanoglu E, Solaroglu I, Surucu HS, Akbiyik F, Beskonakli E (2005) Blockade of sodium channels by phenytoin protects ultrastructure and attenuates lipid peroxidation in experimental spinal cord injury. Acta Neurochir (Wien) 147:405-412; discussion 412. Medline
35. Kiryu-Seo S, Ohno N, Kidd GJ, Komuro H, Trapp BD (2010) Demyelination increases axonal stationary mitochondrial size and the speed of axonal mitochondrial transport. J Neurosci 30:6658-6666. CrossRef Medline
36. Lacomis D (2002) Small-fiber neuropathy. Muscle Nerve 26:173-188. CrossRef Medline
37. Lehmann HC, Chen W, Borzan J, Mankowski JL, Höke A (2011) Mitochondrial dysfunction in distal axons contributes to human immunodeficiency virus sensory neuropathy. Ann Neurol 69:100-110. CrossRef Medline
38. Lehning EJ, Doshi R, Isaksson N, Stys PK, LoPachin RM Jr (1996) Mechanisms of injury-induced calcium entry into peripheral nerve myelinated axons: role of reverse sodium-calcium exchange. J Neurochem 66:493-500. CrossRef Medline
39. Leinster VH, Robson LG, Shortland PJ (2010) Differential effects of riluzole on subpopulations of adult rat dorsal root ganglion neurons in vitro. Neuroscience 166:942-951. CrossRef Medline
40. 2+]i studied in isolated rat cardiomyocytes. J Physiol 496:111-128. Medline
41. 2+) exchange in spinal cord white matter injury at physiological temperature. J Neurophysiol 84:1116-1119. Medline
42. Lingor P, Koch JC, Tönges L, Bähr M (2012) Axonal degeneration as a therapeutic target in the CNS. Cell Tissue Res 349:289-311. CrossRef Medline
43. Malik RA, Masson EA, Sharma AK, Lye RH, Ah-See AK, Compton AM, Tomlinson DR, Hanley SP, Boulton AJ (1990) Hypoxic neuropathy: relevance to human diabetic neuropathy. Diabetologia 33:311-318. CrossRef Medline
44. Millecamps S, Julien JP (2013) Axonal transport deficits and neurodegenerative diseases. Nat Rev Neurosci 14:161-176. CrossRef Medline
45. Morsali D, Bechtold D, Lee W, Chauhdry S, Palchaudhuri U, Hassoon P, Snell DM, Malpass K, Piers T, Pocock J, Roach A, Smith KJ (2013) Safinamide and flecainide protect axons and reduce microglial activation in models of multiple sclerosis. Brain 136:1067-1082. CrossRef Medline
46. 2+ in toxic cell killing. Trends Pharmacol Sci 10:281-285. CrossRef Medline
47. Pardo CA, McArthur JC, Griffin JW (2001) HIV neuropathy: insights in the pathology of HIV peripheral nerve disease. J Peripher Nerv Syst 6:21-27. CrossRef Medline
48. Pareyson D, Marchesi C (2009) Diagnosis, natural history, and management of Charcot-Marie-Tooth disease. Lancet Neurol 8:654-667. CrossRef Medline
49. Park JY, Jang SY, Shin YK, Koh H, Suh DJ, Shinji T, Araki T, Park HT (2013) Mitochondrial swelling and microtubule depolymerization are associated with energy depletion in axon degeneration. Neuroscience 238:258-269. CrossRef Medline
50. Pavlakis PP, Alexopoulos H, Kosmidis ML, Mamali I, Moutsopoulos HM, Tzioufas AG, Dalakas MC (2012) Peripheral neuropathies in Sjogren's syndrome: a critical update on clinical features and pathogenetic mechanisms. J Autoimmun 39:27-33. CrossRef Medline
51. Persson AK, Black JA, Gasser A, Cheng X, Fischer TZ, Waxman SG (2010) Sodium-calcium exchanger and multiple sodium channel isoforms in intra-epidermal nerve terminals. Mol Pain 6:84. CrossRef Medline
52. Persson AK, Liu S, Faber CG, Merkies IS, Black JA, Waxman SG (2013) Neuropathy-associated Na(V) 1.7 variant I228M impairs integrity of dorsal root ganglion neuron axons. Ann Neurol 73:140-145. CrossRef Medline
53. Press C, Milbrandt J (2008) Nmnat delays axonal degeneration caused by mitochondrial and oxidative stress. J Neurosci 28:4861-4871. CrossRef Medline
54. Sheng ZH, Cai Q (2012) Mitochondrial transport in neurons: impact on synaptic homeostasis and neurodegeneration. Nat Rev Neurosci 13:77-93. CrossRef Medline
55. Shields SD, Ahn HS, Yang Y, Han C, Seal RP, Wood JN, Waxman SG, Dib- Hajj SD (2012) Na(v)1.8 expression is not restricted to nociceptors in mouse peripheral nervous system. Pain 153:2017-2030. CrossRef Medline
56. Stirling DP, Stys PK (2010) Mechanisms of axonal injury: internodal nanocomplexes and calcium deregulation. Trends Mol Med 16:160-170. CrossRef Medline
57. 2+ exchanger. J Neurosci 12:430-439. Medline
58. Tavee J, Zhou L (2009) Small fiber neuropathy: a burning problem. Cleve Clin J Med 76:297-305. CrossRef Medline
59. Wang JT, Medress ZA, Barres BA (2012) Axon degeneration: molecular mechanisms of a self-destruction pathway. J Cell Biol 196:7-18. CrossRef Medline
60. Wang MS, Wu Y, Culver DG, Glass JD (2000) Pathogenesis of axonal degeneration: parallels between Wallerian degeneration and vincristine neuropathy. J Neuropathol Exp Neurol 59:599-606. Medline
61. 2+ exchanger inhibitors. J Pharmacol Sci 102:7-16. CrossRef Medline
62. Waxman SG (2006) Axonal conduction and injury in multiple sclerosis: the role of sodium channels. Nat Rev Neurosci 7:932-941. CrossRef Medline
63. Waxman SG, Black JA, Kocsis JD, Ritchie JM (1989) Low density of sodium channels supports action potential conduction in axons of neonatal rat optic nerve. Proc Natl Acad Sci U S A 86:1406-1410. CrossRef Medline
64. Werth JL, Usachev YM, Thayer SA (1996) Modulation of calcium efflux from cultured rat dorsal root ganglion neurons. J Neurosci 16:1008-1015. Medline
65. Zambonin JL, Zhao C, Ohno N, Cambell GR, Engelham S, Ziabreva I, Schwartz N, Lee SE, Frischer JM, Turnbull DM, Trapp BD, Lassmann H, Franklin RJ, Mahad DJ (2011) Increased mitochondrial content in remyelinated axons: implications for multiple sclerosis. Brain 13:1901-1913. CrossRef Medline
66. Züchner S, Mersiyanova IV, Muglia M, Bissar-Tadmouri N, Rochelle J, Dadali EL, Zappia M, Nelis E, Patitucci A, Senderek J, Parman Y, Evgrafov O, Jonghe PD, Takahashi Y, Tsuji S, Pericak-Vance MA, Quattrone A, Battaloglu E, Polyakov AV, Timmerman V, et al. (2004) Mutations in the mitochondrial GTPase mitofusin 2 cause Charcot-Marie-Tooth neuropathy type 2A. Nat Genet 36:449-451. CrossRef Medline